The β isoform of the catalytic subunit of protein phosphatase 2B restrains platelet function by suppressing outside-in αIIbβ3 integrin signaling

Journal of Thrombosis and Haemostasis

Volumn 12, Issue 12, 2014, Pages 2089-2101

  Khatlani, T ^a   Pradhan, S ^a   Da, Q ^a   Gushiken, F C ^a,d   Bergeron, A L ^a   Langlois, K W ^a   Molkentin, J D ^b   Rumbaut, R E ^a,c   Vijayan, K V ^a,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

Author keywords

Beta(3) integrin; Fibrinogen; Platelet aggregation; Platelets; Protein serine threonine phosphatase

Indexed keywords

ALPHA2B BETA3 INTEGRIN; CALCINEURIN; CYCLOSPORIN A; FIBRINOGEN; FILAMIN A; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE; TACROLIMUS; UNCLASSIFIED DRUG; CHLORIDE; FERRIC CHLORIDE; FERRIC ION; FIBRINOGEN RECEPTOR; ISOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CLOT RETRACTION; CAROTID ARTERY OBSTRUCTION; CELL ADHESION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVE SITE; ENZYME ACTIVITY; FEMALE; FIBRIN CLOT; HUMAN; HUMAN CELL; KIDNEY CELL; MALE; MOUSE; NONHUMAN; THROMBOCYTE; THROMBOCYTE FUNCTION; THROMBOSIS; WILD TYPE; ANIMAL; CAROTID ARTERY; CHEMISTRY; CYTOLOGY; FLOW CYTOMETRY; HEK293 CELL LINE; METABOLISM; PATHOPHYSIOLOGY; PHENOTYPE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; THROMBOCYTE AGGREGATION; TRANSGENIC MOUSE;

ANIMALS; BLOOD PLATELETS; CALCINEURIN; CAROTID ARTERIES; CATALYTIC DOMAIN; CELL ADHESION; CHLORIDES; FEMALE; FERRIC COMPOUNDS; FIBRINOGEN; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; MALE; MICE; MICE, TRANSGENIC; PHENOTYPE; PHOSPHORYLATION; PLATELET AGGREGATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; THROMBOSIS;

EID: 84916881119     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12761     Document Type: Article

References (38)

1. Varga-Szabo D, Braun A, Nieswandt B. Calcium signaling in platelets. J Thromb Haemost 2009; 7: 1057-66.
2. Azam M, Andrabi SS, Sahr KE, Kamath L, Kuliopulos A, Chishti AH. Disruption of the mouse mu-calpain gene reveals an essential role in platelet function. Mol Cell Biol 2001; 21: 2213-20.
3. Konopatskaya O, Gilio K, Harper MT, Zhao Y, Cosemans JM, Karim ZA, Whiteheart SW, Molkentin JD, Verkade P, Watson SP, Heemskerk JW, Poole AW. PKCα regulates platelet granule secretion and thrombus formation in mice. J Clin Invest 2009; 119: 399-407.
4. Buensuceso CS, Obergfell A, Soriani A, Eto K, Kiosses WB, Arias-Salgado EG, Kawakami T, Shattil SJ. Regulation of Outside-in signaling in platelets by integrin-associated protein kinase Cβ. J Biol Chem 2005; 280: 644-53.
5. Shibasaki F, Hallin U, Uchino H. Calcineurin as a multifunctional regulator. J Biochem 2002; 131: 1-15.
6. Liu J, Farmer JD Jr, Lane WS, Friedman J, Weissman I, Schreiber SL. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 1991; 66: 807-15.
7. Zaslavsky A, Chou ST, Schadler K, Lieberman A, Pimkin M, Kim YJ, Baek KH, Aird WC, Weiss MJ, Ryeom S. The calcineurin-NFAT pathway negatively regulates megakaryopoiesis. Blood 2013; 121: 3205-15.
8. Bueno OF, Brandt EB, Rothenberg ME, Molkentin JD. Defective T cell development and function in calcineurin A β -deficient mice. Proc Natl Acad Sci USA 2002; 99: 9398-403.
9. 3 function. PLoS One 2009; 4: e8304.
10. Nolasco LH, Gushiken FC, Turner NA, Khatlani TS, Pradhan S, Dong JF, Moake JL, Vijayan KV. Protein phosphatase 2B inhibition promotes the secretion of von Willebrand factor from endothelial cells. J Thromb Haemost 2009; 7: 1009-18.
11. 3 enhances outside-in signaling and adhesive functions. J Clin Invest 2000; 105: 793-802.
12. 3 integrin signalling-dependent functions. Thromb Haemost 2013; 109: 118-26.
13. Dasgupta SK, Le A, Chavakis T, Rumbaut RE, Thiagarajan P. Developmental endothelial locus-1 (Del-1) mediates clearance of platelet microparticles by the endothelium. Circulation 2012; 125: 1664-72.
14. Steinmann B, Bruckner P, Superti-Furga A. Cyclosporin A slows collagen triple-helix formation in vivo: indirect evidence for a physiologic role of peptidyl-prolyl cis-trans-isomerase. J Biol Chem 1991; 266: 1299-303.
15. Jobe SM, Wilson KM, Leo L, Raimondi A, Molkentin JD, Lentz SR, Di PJ. Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood 2008; 111: 1257-65.
16. 3 with Src kinase. Blood 2008; 112: 592-602.
17. 3 signaling in platelets. Blood 2009; 113: 3585-92.
18. Flevaris P, Li Z, Zhang G, Zheng Y, Liu J, Du X. Two distinct roles of mitogen-activated protein kinases in platelets and a novel Rac1-MAPK-dependent integrin outside-in retractile signaling pathway. Blood 2009; 113: 893-901.
19. Mazharian A, Roger S, Berrou E, Adam F, Kauskot A, Nurden P, Jandrot-Perrus M, Bryckaert M. Protease-activating receptor-4 induces full platelet spreading on a fibrinogen matrix: involvement of ERK2 and p38 and Ca2+ mobilization. J Biol Chem 2007; 282: 5478-87.
20. Garcia E, Stracher A, Jay D. Calcineurin dephosphorylates the C-terminal region of filamin in an important regulatory site: a possible mechanism for filamin mobilization and cell signaling. Arch Biochem Biophys 2006; 446: 140-50.
21. Nakamura F, Stossel TP, Hartwig JH. The filamins: organizers of cell structure and function. Cell Adh Migr 2011; 5: 160-9.
22. Legate KR, Fassler R. Mechanisms that regulate adaptor binding to β-integrin cytoplasmic tails. J Cell Sci 2009; 122: 187-98.
23. Pfaff M, Liu S, Erle DJ, Ginsberg MH. Integrin β cytoplasmic domains differentially bind to cytoskeletal proteins. J Biol Chem 1998; 273: 6104-9.
24. Calderwood DA, Huttenlocher A, Kiosses WB, Rose DM, Woodside DG, Schwartz MA, Ginsberg MH. Increased filamin binding to β-integrin cytoplasmic domains inhibits cell migration. Nat Cell Biol 2001; 3: 1060-8.
25. Grace AA, Barradas MA, Mikhailidis DP, Jeremy JY, Moorhead JF, Sweny P, Dandona P. Cyclosporine A enhances platelet aggregation. Kidney Int 1987; 32: 889-95.
26. Fernandes JB, Naik UP, Markell MS, Kornecki E. Comparative investigation of the effects of the immunosuppressants cyclosporine A, cyclosporine G, and FK-506 on platelet activation. Cell Mol Biol Res 1993; 39: 265-74.
27. Tomasiak M, Rusak T, Gacko M, Stelmach H. Cyclosporine enhances platelet procoagulant activity. Nephrol Dial Transplant 2007; 22: 1750-6.
28. Su Z, Xin S, Li J, Guo J, Long X, Cheng J, Wei Q. A new function for the calcineurin β subunit: antiplatelet aggregation and anticoagulation. IUBMB Life 2011; 63: 1037-44.
29. Gooch JL, Toro JJ, Guler RL, Barnes JL. Calcineurin A-α but not A-β is required for normal kidney development and function. Am J Pathol 2004; 165: 1755-65.
30. Graef IA, Chen F, Chen L, Kuo A, Crabtree GR. Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell 2001; 105: 863-75.
31. Rosado JA, Pariente JA, Salido GM, Redondo PC. SERCA2b activity is regulated by cyclophilins in human platelets. Arterioscler Thromb Vasc Biol 2010; 30: 419-25.
32. Lim HW, New L, Han J, Molkentin JD. Calcineurin enhances MAPK phosphatase-1 expression and p38 MAPK inactivation in cardiac myocytes. J Biol Chem 2001; 276: 15913-9.
33. Berrou E, Adam F, Lebret M, Fergelot P, Kauskot A, Coupry I, Jandrot-Perrus M, Nurden A, Favier R, Rosa JP, Goizet C, Nurden P, Bryckaert M. Heterogeneity of platelet functional alterations in patients with filamin A mutations. Arterioscler Thromb Vasc Biol 2013; 33: e11-8.
34. Chen M, Stracher A. In situ phosphorylation of platelet actin-binding protein by cAMP-dependent protein kinase stabilizes it against proteolysis by calpain. J Biol Chem 1989; 264: 14282-9.
35. Jay D, Garcia EJ, de la Luz Ibarra M. In situ determination of a PKA phosphorylation site in the C-terminal region of filamin. Mol Cell Biochem 2004; 260: 49-53.
36. Chen HS, Kolahi KS, Mofrad MR. Phosphorylation facilitates the integrin binding of filamin under force. Biophys J 2009; 97: 3095-104.
37. Vadlamudi RK, Li F, Adam L, Nguyen D, Ohta Y, Stossel TP, Kumar R. Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat Cell Biol 2002; 4: 681-90.
38. 3. EMBO J 1997; 16: 6414-25.